Developing RNA aptamers for potential treatment of neurological diseases

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Craig PN. Proceedings: Comparison of Hansch and Free–Wilson methods for structure–activity correlation. Cancer Chemother. Rep. 4(4), 39 (1974).
  CASGoogle Scholar
• 2 Anderson AC. The process of structure-based drug design. Chem. Biol. 10(9), 787–797 (2003). • A general approach for using structure-based drug design is presented.
  Medline CASGoogle Scholar
• 3 Bajorath J. Computer-aided drug discovery. F1000Res 4, doi:10.12688/f1000research.6653.1 (2015). • A general approach for using computer-aided, computational chemistry in drug design is presented.
  MedlineGoogle Scholar
• 4 Kennedy JP, Williams L, Bridges TM, Daniels RN, Weaver D, Lindsley CW. Application of combinatorial chemistry science on modern drug discovery. J. Comb. Chem. 10(3), 345–354 (2008).
  Medline CASGoogle Scholar
• 5 Liu R, Li X, Lam KS. Combinatorial chemistry in drug discovery. Curr. Opin. Chem. Biol. 38, 117–126 (2017).
  Medline CASGoogle Scholar
• 6 Franzini RM, Neri D, Scheuermann J. DNA-encoded chemical libraries: advancing beyond conventional small-molecule libraries. Acc. Chem. Res. 47(4), 1247–1255 (2014).
  Medline CASGoogle Scholar
• 7 Shoichet BK. Virtual screening of chemical libraries. Nature 432(7019), 862–865 (2004). • This is a comprehensive review in the use of virtual screening in drug discovery.
  Medline CASGoogle Scholar
• 8 Kitchen DB, Decornez H, Furr JR, Bajorath J. Docking and scoring in virtual screening for drug discovery: methods and applications. Nat. Rev. Drug Discov. 3(11), 935–949 (2004).
  Medline CASGoogle Scholar
• 9 Ruddigkeit L, Van Deursen R, Blum LC, Reymond JL. Enumeration of 166 billion organic small molecules in the chemical universe database GDB-17. J. Chem. Inf. Model. 52(11), 2864–2875 (2012).
  Medline CASGoogle Scholar
• 10 Reymond JL. The chemical space project. Acc. Chem. Res. 48(3), 722–730 (2015).
  Medline CASGoogle Scholar
• 11 Scott DE, Bayly AR, Abell C, Skidmore J. Small molecules, big targets: drug discovery faces the protein–protein interaction challenge. Nat. Rev. Drug Discov. 15(8), 533–550 (2016).
  Medline CASGoogle Scholar
• 12 Hermann T, Patel DJ. Adaptive recognition by nucleic acid aptamers. Science 287(5454), 820–825 (2000).
  Medline CASGoogle Scholar
• 13 Ellington AD, Szostak JW. In vitro selection of RNA molecules that bind specific ligands. Nature 346(6287), 818–822 (1990). • This is one of the two original studies in the development of SELEX to isolate useful RNA aptamers; the second study is reference 20.
  Medline CASGoogle Scholar
• 14 Tuerk C, Gold L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249(4968), 505–510 (1990). • This is second, original report in the development of SELEX to isolate useful RNA aptamers; the first paper is reference 19.
  Medline CASGoogle Scholar
• 15 Huang Z, Pei W, Jayaseelan S, Shi H, Niu L. RNA aptamers selected against the GluR2 glutamate receptor channel. Biochemistry 46(44), 12648–12655 (2007).
  Medline CASGoogle Scholar
• 16 Kahsai AW, Wisler JW, Lee J et al. Conformationally selective RNA aptamers allosterically modulate the beta2-adrenoceptor. Nat. Chem. Biol. 12(9), 709–716 (2016).
  Medline CASGoogle Scholar
• 17 Rajendran M, Ellington AD. Selection of fluorescent aptamer beacons that light up in the presence of zinc. Anal. Bioanal. Chem. 390(4), 1067–1075 (2008).
  Medline CASGoogle Scholar
• 18 Ciesiolka J, Yarus M. Small RNA-divalent domains. RNA 2(8), 785–793 (1996).
  Medline CASGoogle Scholar
• 19 Shangguan D, Li Y, Tang Z et al. Aptamers evolved from live cells as effective molecular probes for cancer study. Proc. Natl Acad. Sci. USA 103(32), 11838–11843 (2006).
  Medline CASGoogle Scholar
• 20 Gopinath SC, Hayashi K, Kumar PK. Aptamer that binds to the gD protein of herpes simplex virus 1 and efficiently inhibits viral entry. J. Virol. 86(12), 6732–6744 (2012).
  Medline CASGoogle Scholar
• 21 Cnossen EJ, Silva AG, Marangoni K et al. Characterization of oligonucleotide aptamers targeting the 5’-UTR from dengue virus. Future Med. Chem. 9(6), 541–552 (2017).
  CASGoogle Scholar
• 22 Keefe AD, Pai S, Ellington A. Aptamers as therapeutics. Nat. Rev. Drug Discov. 9(7), 537–550 (2010).
  Medline CASGoogle Scholar
• 23 Huang Z, Pei W, Han Y et al. One RNA aptamer sequence, two structures: a collaborating pair that inhibits AMPA receptors. Nucleic Acids Res. 37(12), 4022–4032 (2009). •• RNA aptamers that share the same length and the sequence, transcribed from the same DNA template in the same transcription reaction, can have different functions by binding to different sites. They act, as a collaborating pair, to competitively inhibit AMPA receptors.
  Medline CASGoogle Scholar
• 24 Wilson DS, Szostak JW. In vitro selection of functional nucleic acids. Annu. Rev. Biochem. 68, 611–647 (1999).
  Medline CASGoogle Scholar
• 25 Bornberg-Bauer E. How are model protein structures distributed in sequence space? Biophys. J. 73(5), 2393–2403 (1997).
  Medline CASGoogle Scholar
• 26 Huynen MA, Stadler PF, Fontana W. Smoothness within ruggedness: the role of neutrality in adaptation. Proc. Natl Acad. Sci. USA 93(1), 397–401 (1996).
  Medline CASGoogle Scholar
• 27 Schultes EA, Bartel DP. One sequence, two ribozymes: implications for the emergence of new ribozyme folds. Science 289(5478), 448–452 (2000).
  Medline CASGoogle Scholar
• 28 Spiegelman S. An approach to the experimental analysis of precellular evolution. Q Rev. Biophys. 4(2), 213–253 (1971).
  Medline CASGoogle Scholar
• 29 Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol. Rev. 51(1), 7–61 (1999).
  Medline CASGoogle Scholar
• 30 Solyom S, Tarnawa I. Non-competitive AMPA antagonists of 2,3-benzodiazepine type. Curr. Pharm. Des. 8(10), 913–939 (2002).
  Medline CASGoogle Scholar
• 31 Noh KM, Yokota H, Mashiko T, Castillo PE, Zukin RS, Bennett MV. Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc. Natl Acad. Sci. USA 102(34), 12230–12235 (2005).
  Medline CASGoogle Scholar
• 32 Conrad KL, Tseng KY, Uejima JL et al. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454(7200), 118–121 (2008).
  Medline CASGoogle Scholar
• 33 Rogawski MA, Hanada T. Preclinical pharmacology of perampanel, a selective non-competitive AMPA receptor antagonist. Acta Neurol. Scand. Suppl. 197, 19–24 (2013).
  MedlineGoogle Scholar
• 34 Zappala M, Grasso S, Micale N, Polimeni S, De Micheli C. Synthesis and structure–activity relationships of 2,3-benzodiazepines as AMPA receptor antagonists. Mini. Rev. Med. Chem. 1(3), 243–253 (2001).
  Medline CASGoogle Scholar
• 35 Gorter JA, Petrozzino JJ, Aronica EM et al. Global ischemia induces downregulation of Glur2 mRNA and increases AMPA receptor-mediated Ca²⁺ influx in hippocampal CA1 neurons of gerbil. J. Neurosci. 17(16), 6179–6188 (1997).
  Medline CASGoogle Scholar
• 36 Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I, Kwak S. Glutamate receptors: RNA editing and death of motor neurons. Nature. 427(6977), 801 (2004).
  Medline CASGoogle Scholar
• 37 Newcombe J, Uddin A, Dove R et al. Glutamate receptor expression in multiple sclerosis lesions. Brain Pathol. 18(1), 52–61 (2008).
  MedlineGoogle Scholar
• 38 Honore T, Davies SN, Drejer J et al. Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science 241(4866), 701–703 (1988).
  Medline CASGoogle Scholar
• 39 Armstrong N, Gouaux E. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core. Neuron 28(1), 165–181 (2000). • Reports the first crystal structure for a partial AMPA receptor.
  Medline CASGoogle Scholar
• 40 Topliss JG. Utilization of operational schemes for analog synthesis in drug design. J. Med. Chem. 15(10), 1006–1011 (1972).
  Medline CASGoogle Scholar
• 41 Bausch-Fluck D, Hofmann A, Bock T et al. A mass spectrometric-derived cell surface protein atlas. PLoS ONE. 10(3), e0121314 (2015).
  MedlineGoogle Scholar
• 42 Wurm FM. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat. Biotechnol. 22(11), 1393–1398 (2004).
  Medline CASGoogle Scholar
• 43 Jordan M, Schallhorn A, Wurm FM. Transfecting mammalian cells: optimization of critical parameters affecting calcium–phosphate precipitate formation. Nucleic Acids Res. 24(4), 596–601 (1996).
  Medline CASGoogle Scholar
• 44 Chen C, Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7(8), 2745–2752 (1987).
  Medline CASGoogle Scholar
• 45 Park JS, Wang C, Han Y, Huang Z, Niu L. Potent and selective inhibition of a single alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunit by an RNA aptamer. J. Biol. Chem. 286(17), 15608–15617 (2011). •• Discovery of a single subunti-selective RNA aptamer was described.
  Medline CASGoogle Scholar
• 46 Huang Z, Han Y, Wang C, Niu L. Potent and selective inhibition of the open-channel conformation of AMPA receptors by an RNA aptamer. Biochemistry 49(27), 5790–5798 (2010). •• An RNA aptamer selective to a particular conformation of AMPA receptors can be isolated.
  Medline CASGoogle Scholar
• 47 Jaremko WJ, Huang Z, Wen W, Wu A, Karl N, Niu L. One aptamer, two functions: the full-length aptamer inhibits AMPA receptors, while the short one inhibits both AMPA and kainate receptors. RNA Dis. 4(2), e1560 (2017).
  MedlineGoogle Scholar
• 48 Jaremko WJ, Huang Z, Wen W, Wu A, Karl N, Niu L. Identification and characterization of RNA aptamers: a long aptamer blocks the AMPA receptor and a short aptamer blocks both AMPA and kainate receptors. J. Biol. Chem. 292(18), 7338–7347 (2017).
  Medline CASGoogle Scholar
• 49 Topliss JG. A manual method for applying the Hansch approach to drug design. J. Med. Chem. 20(4), 463–469 (1977).
  Medline CASGoogle Scholar
• 50 Hsu JL, Hung MC. The role of HER2, EGFR, and other receptor tyrosine kinases in breast cancer. Cancer Metastasis Rev. 35(4), 575–588 (2016).
  Medline CASGoogle Scholar
• 51 Charbonnier LM, Janssen E, Chou J et al. Regulatory T-cell deficiency and immune dysregulation, polyendocrinopathy, enteropathy, X-linked-like disorder caused by loss-of-function mutations in LRBA. J. Allergy Clin. Immunol. 135(1), 217–227 (2015).
  Medline CASGoogle Scholar
• 52 Villar-Cheda B, Dominguez-Meijide A, Valenzuela R, Granado N, Moratalla R, Labandeira-Garcia JL. Aging-related dysregulation of dopamine and angiotensin receptor interaction. Neurobiol. Aging 35(7), 1726–1738 (2014).
  Medline CASGoogle Scholar
• 53 Gashaw I, Ellinghaus P, Sommer A, Asadullah K. What makes a good drug target? Drug Discov. Today 17(Suppl.), S24–30 (2012).
  Medline CASGoogle Scholar
• 54 Hendrickson WA. Atomic-level analysis of membrane-protein structure. Nat. Struct. Mol. Biol. 23(6), 464–467 (2016).
  Medline CASGoogle Scholar
• 55 Wallin E, Von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7(4), 1029–1038 (1998).
  Medline CASGoogle Scholar
• 56 Overington JP, Al-Lazikani B, Hopkins AL. How many drug targets are there? Nat. Rev. Drug Discov. 5(12), 993–996 (2006).
  Medline CASGoogle Scholar
• 57 Armstrong N, Sun Y, Chen GQ, Gouaux E. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395(6705), 913–917 (1998).
  Medline CASGoogle Scholar
• 58 Jin R, Banke TG, Mayer ML, Traynelis SF, Gouaux E. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6(8), 803–810 (2003).
  Medline CASGoogle Scholar
• 59 Li G, Pei W, Niu L. Channel-opening kinetics of GluR2Q(flip) AMPA receptor: a laser-pulse photolysis study. Biochemistry 42(42), 12358–12366 (2003).
  Medline CASGoogle Scholar
• 60 Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428(6980), 281–286 (2004).
  Medline CASGoogle Scholar
• 61 Goodsell DS, Olson AJ. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29, 105–153 (2000).
  Medline CASGoogle Scholar
• 62 Que-Gewirth NS, Sullenger BA. Gene therapy progress and prospects: RNA aptamers. Gene Ther. 14(4), 283–291 (2007).
  Medline CASGoogle Scholar
• 63 Fauman EB, Rai BK, Huang ES. Structure-based druggability assessment – identifying suitable targets for small molecule therapeutics. Curr. Opin. Chem. Biol. 15(4), 463–468 (2011).
  Medline CASGoogle Scholar
• 64 Blind M, Blank M. Aptamer Selection technology and recent advances. Mol. Ther. Nucleic Acids 4, e223 (2015).
  MedlineGoogle Scholar
• 65 Hogan JC Jr Combinatorial chemistry in drug discovery. Nat. Biotechnol. 15(4), 328–330 (1997).
  Medline CASGoogle Scholar
• 66 Dolle RE. Historical overview of chemical library design. Methods Mol. Biol. 685, 3–25 (2011).
  Medline CASGoogle Scholar
• 67 Scheuermann J, Neri D. DNA-encoded chemical libraries: a tool for drug discovery and for chemical biology. Chembiochem 11(7), 931–937 (2010).
  Medline CASGoogle Scholar
• 68 Neri D, Lerner RA. DNA-encoded chemical libraries: a selection system based on endowing organic compounds with amplifiable information. Annu. Rev. Biochem. 87, 479–502 (2018).
  Medline CASGoogle Scholar
• 69 Sanger F. Sequences, sequences, and sequences. Annu. Rev. Biochem. 57, 1–28 (1988).
  Medline CASGoogle Scholar
• 70 Meldrum C, Doyle MA, Tothill RW. Next-generation sequencing for cancer diagnostics: a practical perspective. Clin. Biochem. Rev. 32(4), 177–195 (2011).
  MedlineGoogle Scholar
• 71 Joachimiak A. High-throughput crystallography for structural genomics. Curr. Opin. Struct. Biol. 19(5), 573–584 (2009).
  Medline CASGoogle Scholar
• 72 Gordon JW, Scangos GA, Plotkin DJ, Barbosa JA, Ruddle FH. Genetic transformation of mouse embryos by microinjection of purified DNA. Proc. Natl Acad. Sci. USA 77(12), 7380–7384 (1980).
  Medline CASGoogle Scholar
• 73 Ziegler A, Koch A, Krockenberger K, Grosshennig A. Personalized medicine using DNA biomarkers: a review. Hum. Genet. 131(10), 1627–1638 (2012).
  Medline CASGoogle Scholar
• 74 Scannell JW, Blanckley A, Boldon H, Warrington B. Diagnosing the decline in pharmaceutical R&D efficiency. Nat. Rev. Drug Discov. 11(3), 191–200 (2012).
  Medline CASGoogle Scholar
• 75 Lieberman J. Tapping the RNA world for therapeutics. Nat. Struct. Mol. Biol. 25(5), 357–364 (2018).
  Medline CASGoogle Scholar
• 76 Yoon S, Rossi JJ. Aptamers: Uptake mechanisms and intracellular applications. Adv. Drug Deliv. Rev. 134, 22–35 (2018).
  Medline CASGoogle Scholar
• 77 Morrissey DV, Lockridge JA, Shaw L et al. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol. 23(8), 1002–1007 (2005).
  Medline CASGoogle Scholar
• 78 Healy JM, Lewis SD, Kurz M et al. Pharmacokinetics and biodistribution of novel aptamer compositions. Pharm. Res. 21(12), 2234–2246 (2004).
  Medline CASGoogle Scholar
• 79 Gomes De Castro MA, Hobartner C, Opazo F. Aptamers provide superior stainings of cellular receptors studied under super-resolution microscopy. PLoS ONE 12(2), e0173050 (2017).
  MedlineGoogle Scholar
• 80 Pieken WA, Olsen DB, Benseler F, Aurup H, Eckstein F. Kinetic characterization of ribonuclease-resistant 2’-modified hammerhead ribozymes. Science 253(5017), 314–317 (1991).
  Medline CASGoogle Scholar
• 81 Sawadogo M, Roeder RG. Factors involved in specific transcription by human RNA polymerase II: analysis by a rapid and quantitative in vitro assay. Proc. Natl Acad. Sci. USA 82(13), 4394–4398 (1985).
  Medline CASGoogle Scholar
• 82 Cummins LL, Owens SR, Risen LM et al. Characterization of fully 2’-modified oligoribonucleotide hetero- and homoduplex hybridization and nuclease sensitivity. Nucleic Acids Res. 23(11), 2019–2024 (1995).
  Medline CASGoogle Scholar
• 83 Brody EN, Gold L. Aptamers as therapeutic and diagnostic agents. J. Biotechnol. 74(1), 5–13 (2000).
  Medline CASGoogle Scholar
• 84 Dass CR, Saravolac EG, Li Y, Sun LQ. Cellular uptake, distribution, and stability of 10–23 deoxyribozymes. Antisense Nucleic Acid Drug Dev. 12(5), 289–299 (2002).
  Medline CASGoogle Scholar
• 85 Heidenreich O, Pieken W, Eckstein F. Chemically modified RNA: approaches and applications. Faseb J. 7(1), 90–96 (1993).
  Medline CASGoogle Scholar
• 86 Ng EW, Shima DT, Calias P, Cunningham ET Jr, Guyer DR, Adamis AP. Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat Rev Drug Discov. 5(2), 123–132 (2006).
  Medline CASGoogle Scholar
• 87 Tucker CE, Chen LS, Judkins MB, Farmer JA, Gill SC, Drolet DW. Detection and plasma pharmacokinetics of an anti-vascular endothelial growth factor oligonucleotide-aptamer (NX1838) in rhesus monkeys. J. Chromatogr. B. Biomed. Sci. Appl. 732(1), 203–212 (1999).
  Medline CASGoogle Scholar
• 88 Huang Z, Wen W, Wu A, Niu L. Chemically modified, alpha-amino-3-hydroxy-5-methyl-4-isoxazole (AMPA) receptor RNA aptamers designed for in vivo use. ACS Chem. Neurosci. 8(11), 2437–2445 (2017). •• Making chemically modified RNA aptamers by enzymatic transcription reaction is presented; these RNA aptamers are sufficiently stable to be used in vivo.
  Medline CASGoogle Scholar
• 89 Cazenave C, Uhlenbeck OC. RNA template-directed RNA synthesis by T7 RNA polymerase. Proc. Natl Acad. Sci. USA 91(15), 6972–6976 (1994).
  Medline CASGoogle Scholar
• 90 Ruckman J, Green LS, Beeson J et al. 2’-Fluoropyrimidine RNA-based aptamers to the 165-amino acid form of vascular endothelial growth factor (VEGF165). Inhibition of receptor binding and VEGF-induced vascular permeability through interactions requiring the exon 7-encoded domain. J. Biol. Chem. 273(32), 20556–20567 (1998).
  Medline CASGoogle Scholar
• 91 Yaksh TL, Rudy TA. Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 17(6), 1031–1036 (1976).
  Medline CASGoogle Scholar
• 92 Bustamante D, Paeile C, Willer JC, Le Bars D. Effects of intrathecal or intracerebroventricular administration of nonsteroidal anti-inflammatory drugs on a C-fiber reflex in rats. J. Pharmacol. Exp. Ther. 281(3), 1381–1391 (1997).
  Medline CASGoogle Scholar
• 93 Luo MC, Zhang DQ, Ma SW et al. An efficient intrathecal delivery of small interfering RNA to the spinal cord and peripheral neurons. Mol. Pain 1, 29 (2005).
  MedlineGoogle Scholar
• 94 Storkebaum E, Lambrechts D, Dewerchin M et al. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat. Neurosci. 8(1), 85–92 (2005).
  Medline CASGoogle Scholar
• 95 Staquet H, Dupoiron D, Nader E, Menei P. Intracerebroventricular pain treatment with analgesic mixtures including ziconotide for intractable pain. Pain Phys. 19(6), E905–E915 (2016).
  MedlineGoogle Scholar
• 96 Kesselheim AS, Hwang TJ, Franklin JM. Two decades of new drug development for central nervous system disorders. Nat. Rev. Drug Discov. 14(12), 815–816 (2015).
  Medline CASGoogle Scholar
• 97 Pangalos MN, Schechter LE, Hurko O. Drug development for CNS disorders: strategies for balancing risk and reducing attrition. Nat. Rev. Drug Discov. 6(7), 521–532 (2007).
  Medline CASGoogle Scholar
• 98 Pankevich DE, Altevogt BM, Dunlop J, Gage FH, Hyman SE. Improving and accelerating drug development for nervous system disorders. Neuron 84(3), 546–553 (2014).
  Medline CASGoogle Scholar
• 99 Santos R, Ursu O, Gaulton A et al. A comprehensive map of molecular drug targets. Nat. Rev. Drug Discov. 16(1), 19–34 (2017).
  Medline CASGoogle Scholar
• 100 Kreuter J. Drug delivery to the central nervous system by polymeric nanoparticles: what do we know? Adv. Drug Deliv. Rev. 71, 2–14 (2014).
  Medline CASGoogle Scholar